World J Gastrointest Endosc 2016 November 16; 8(19): 709-715 ISSN 1948-5190 (online)
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ORIGINAL ARTICLE Prospective Study
Post-endoscopic retrograde cholangiopancreatography pancreatitis: Risk factors and predictors of severity Ayman El Nakeeb, Ehab El Hanafy, Tarek Salah, Ehab Atef, Hosam Hamed, Ahmad M Sultan, Emad Hamdy, Mohamed Said, Ahmed A El Geidie, Tharwat Kandil, Mohamed El Shobari, Gamal El Ebidy Received: June 5, 2016 Peer-review started: June 6, 2016 First decision: July 20, 2016 Revised: July 27, 2016 Accepted: August 27, 2016 Article in press: August 29, 2016 Published online: November 16, 2016
Ayman El Nakeeb, Ehab El Hanafy, Tarek Salah, Ehab Atef, Hosam Hamed, Ahmad M Sultan, Emad Hamdy, Mohamed Said, Ahmed A El Geidie, Tharwat Kandil, Mohamed El Shobari, Gamal El Ebidy, Gastroenterology Surgical Center, Mansoura University, Mansoura 35516, Egypt Author contributions: El Nakeeb A designed the research; El Nakeeb A, El Hanafy E, Salah T, Atef E, Hamed H, Sultan AM, Hamdy E, Said M, El Geidie AA, KandilT, El Shobari M and El Ebidy G performed the research; El Nakeeb A and Said M analyzed data; El Nakeeb A and Hamed H wrote the paper.
Abstract AIM To detect risk factors for post-endoscopic retrograde cholangiopancreatography (ERCP) pancreatitis (PEP) and investigate the predictors of its severity.
Institutional review board statement: This study was approved by the institutional review board of Mansoura University. Informed consent statement: All patients underwent ERCP after a careful explanation of the nature of the disease and possible complications.
METHODS This is a prospective cohort study of all patients who underwent ERCP. Pre-ERCP data, intraoperative data, and post-ERCP data were collected.
Conflict-of-interest statement: There are no potential conflicts of interest relevant to this article. Data sharing statement: No additional data are available.
RESULTS The study population consisted of 996 patients. Their mean age at presentation was 58.42 (± 14.72) years, and there were 454 male and 442 female patients. Overall, PEP occurred in 102 (10.2%) patients of the study population; eighty (78.4%) cases were of mild to moderate degree, while severe pancreatitis occurred in 22 (21.6%) patients. No hospital mortality was reported for any of PEP patients during the study duration. Age less than 35 years (P = 0.001, OR = 0.035), narrower common bile duct (CBD) diameter (P = 0.0001) and in creased number of pancreatic cannulations (P = 0.0001) were independent risk factors for the occurrence of PEP.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/ licenses/by-nc/4.0/ Manuscript source: Unsolicited manuscript Correspondence to: Ayman El Nakeeb, Associate Professor, Gastroenterology Surgical Center, Mansoura University, El Gomhouria St, Mansoura 35516, Egypt.
[email protected] Telephone: +2-50-2353430 Fax: +2-50-2243220
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CONCLUSION PEP is the most frequent and devastating complication after ERCP. Age less than 35 years, narrower median CBD diameter and increased number of pancreatic
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El Nakeeb et al . Post-ERCP pancreatitis [9]
cannulations are independent risk factors for the occurrence of PEP. Patients with these risk factors are candidates for prophylactic and preventive measures against PEP.
remain unclear . The aim of this study was to detect risk factors for PEP and investigate the predictors of its severity in a tertiary high volume referral surgical center in Middle East in Egypt.
Key words: Pancreatitis; Obstructive jaundice; Endoscopic retrograde cholangiopancreatography
MATERIALS AND METHODS This is a prospective cohort study of all patients who underwent ERCP between August 2012 and September 2014. Excluded patients were those who presented with obstructed stent, active pancreatitis, previous endoscopic sphinterotomy, biliary complications after liver transplantation, dye allergy, pregnancy, or mental disability. Patients were admitted 24 h before the procedure. Baseline laboratory assessment of liver functions, blood count and serum amylase level were done prior to ERCP. No pre-ERCP treatment was used to decrease the risk of PEP. In our center, ERCP is performed under general anesthesia with endotracheal intubation in left semi prone position with monitoring of oxygen saturation, heart rate, and blood pressure. The procedure was performed by experienced endoscopists who had performed at least 1500 ERCPs over the last 10 years. Selective bile duct cannulation was carried out in all patients, but pancreatic duct cannulation was performed when necessary. When three or more attempts were needed due to difficulty in cannulation, precut papillotomy was selectively performed. In addition, endoscopic papillotomy for stone extraction using balloon, basket and mechanical lithotripsy, bile duct placement of either plastic or self-expanding metallic stent, as well as brush cytology and dilation, were per formed when indicted. Pancreatic duct stenting was not used to minimize PEP in our practice. ERCP data were recorded in a standardized manner including all potential risk factors for PEP. Patients were hospitalized for 24 h after the procedure and observed for symptoms and signs of post-ERCP complications. Complete blood picture and serum amylase level were determined routinely after 6 h and 24 h. PEP was defined and classified according to the [10] consensus definition and grading system . PEP was defined as new or worsened abdominal pain together with a serum amylase level at least three times normal at more than 24 h after ERCP and necessitating hospi talization for more than one night. PEP was graded according to the length of hospital stay and the need for intervention. Mild PEP required hospitalization for 2-3 nights, moderate PEP required hospitalization for 4-10 nights, and severe pancreatitis required hospitalization for more than 10 d, or required intervention or was com [10] plicated by pseudocyst . Descriptive data are presented as means and standard deviation or medians with range according to the data distribution. Comparison of means was done 2 by χ test for categorical data or Student’s t test for continuous data. Difference was considered significant when a P-value was less than 0.05. Independent risk factors for PEP were assessed by multiple logistic
© The Author(s) 2016. Published by Baishideng Publishing Group Inc. All rights reserved.
Core tip: Endoscopic retrograde cholangiopancreato graphy (ERCP) is increasingly used for therapeutic management of various biliary and pancreatic diseases. However, ERCP is not a procedure without morbidities. Post-ERCP pancreatitis (PEP) remains the most devastating and frequent complication after ERCP. Identification of risk factors for PEP helps adopt prophylactic measures in high risk patients and early discharge in low risk patients. Age less than 35 years, narrower median common bile duct diameter and increased number of pancreatic cannulations were identified to be independent risk factors for the occurrence of PEP. El Nakeeb A, El Hanafy E, Salah T, Atef E, Hamed H, Sultan AM, Hamdy E, Said M, El Geidie AA, Kandil T, El Shobari M, El Ebidy G. Post-endoscopic retrograde cholangiopancreatography pancreatitis: Risk factors and predictors of severity. World J Gastrointest Endosc 2016; 8(19): 709-715 Available from: URL: http://www.wjgnet.com/1948-5190/full/v8/i19/709.htm DOI: http://dx.doi.org/10.4253/wjge.v8.i19.709
INTRODUCTION Endoscopic retrograde cholangiopancreatography (ERCP) is increasingly used for therapeutic management of va [1] rious biliary and pancreatic diseases . However, ERCP [2] is not a procedure without morbidities . Post-ERCP pancreatitis (PEP) remains the most common and serious [3] complication after ERCP . The reported incidence of PEP [4,5] is around 5% . This rate may increase up to 20%-40% in high risk patients. Although the majority of PEP cases are of mild degree, it can be severe and life threatening [6] in a substantial proportion of cases . Identification of risk factors for PEP helps adopt prophylactic measures in high risk patients and early [1,7,8] discharge in low risk patients . Being convinced with a number of patient-related risk factors, some gastroen terologists and surgeons prefer adoption of alternative management strategies for ERCP whenever possible in high risk patients. Similarly, some endoscopists try to avoid procedure-related risk factors to increases the safety of the procedure. All these factors make identification of risk factors for PEP be of paramount importance for the practice of ERCP. Many patient and procedure related factors have been suggested to be associated with increased likelihood of [8] PEP . The trigger mechanism and pathogenesis for PEP
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El Nakeeb et al . Post-ERCP pancreatitis jaundice due to periampullary tumor (n = 460, 46.2%) or hilar cholangiocarcinoma (n = 2, 0.2%), calcular obstructive jaundice (n = 512, 51.4%), benign biliary stricture (n = 10, 1.0%), and post-cholecystectomy biliary leakage (n = 12, 1.2%). The mean age at presentation was 58.42 (± 14.727) years. There were 554 male in comparison to 442 female patients, with a male to female ratio of 1.3:1. Overall, PEP occurred in 102 (10.2%) patients of the study population. Eighty (78.4%) cases were of mild to moderate degree, while severe pancreatitis occurred in 22 (21.6%) patients. The median length of hospital stay in patients with pancreatitis was 3 d (range, 2-15 d). No hospital mortality was reported for any of PEP patients during the study duration. Univariate analysis showed that patient age and narrower CBD diameter are statistically significant patient-related risk factors associated with occurrence and severity of PEP, while increased number of cannulation attempts and pancreatic cannulation more than three times were significant procedure-related risk factors associated with occurrence and severity of PEP. Indication for ERCP was not significantly associated with occurrence of pancreatitis (P = 0.4), but it was significantly associated with the severity of PEP (P = 0.009) (Tables 1 and 2). Multivariate analysis after binary logistic regression analysis revealed that patient age less than 35 years (P = 0.001, OR = 0.035), narrower median CBD diameter (P = 0.0001) and increased number of pancreatic can nulations (P = 0.0001) were independent risk factors for the occurrence of PEP (Table 3).
Table 1 Risk factors for pancreatitis after endoscopic retrograde cholangiopancreatography n (%) No pancreatitis Pancreatitis P -value Patient related factors Median age (yr) Age group < 35 > 35 Sex Male Female Median serum bilirubin (mg%) 2 Median CBD diameter (mm) < 10 > 10 Indication for ERCP Malignant Benign Type of papilla Normal Atrophic Pregnant Tumour Redundant Juxtadivericular Small Long Procedure related factors Number of cannulation attempts 3 times Method of cannulation Conventional Precut Biliary sphincter balloon dilatation No Yes
894 (89.9)
102 (10.2)
60
48
0.0001
32 (7.2) 415 (92.8)
20 (39.2) 31 (60.8)
0.0001
510 (57) 384 (43) 10.6 124 (88.6) 770 (90) 16 70 (7.8) 824 (92.2)
44 (43.1) 58 (56.9) 12.5 16 (11.4) 86 (10) 10 58 (56.9) 44 (43.1)
0.05
402 (45) 492 (55)
40 (39.2) 62 (60.8)
0.43
540 (60.4) 18 (2) 68 (7.6) 64 (7.2) 66(7.4) 68 (7.6) 60 (6.6) 10 (1.1)
56 (54.9) 8 (7.8) 2 (2) 4 (3.9) 12 (11.8) 16 (15.7) 2 (2) 2 (2)
0.01
660 (73.9) 234 (26.1) 0
58 (56.9) 44 (43.1) 2
0.01 0.0001
864 (96.6) 28 (3.4)
60 (58.8) 42 (41.2)
0.0001
640 (89.4) 252 (90.6)
76 (10.6) 26 (9.4)
0.7
654 (73.2) 240 (26.8)
86 (84.3) 16 (15.7)
0.08
0.76 0.72 0.0001 0.0001
DISCUSSION PEP is the most common and serious complication after [8] ERCP . PEP is associated with higher morbidity and mortality beside its effect in increasing the consumption [11] of hospital resources . Identification of clinical and procedural correlates for PEP is of crucial importance in the practice of ERCP. It affects the medical decision regarding patient choice, adoption of pharmacological prophylactic measures, avoidance of procedural risk factors, and determination of the time of discharge [1,7,8] after the procedure . Risk factors for PEP have been a matter of controversy and the pathogenesis of PEP [9,11] is not fully understood yet . This study reports risk factors for PEP according to the experience of a tertiary high volume surgical center in Egypt. Despite advanced accessories and novel techniques in ERCP, complication rate after ERCP remained un [7,12] changed over the last decade . According to previous reports, the incidence of PEP ranges from 5% to 40%. This great discrepancy in the reported rates can be attributed to heterogeneity of the definition of PEP and its grading system, variability in data collection, inclusion of diagnostic ERCP in the study, and difference [13] in expertise among endoscopists . The incidence of PEP in this cohort was 10.2% with adoption of the consensus [10] definition of PEP . Mild to moderate PEP occurred in 80
CBD: Common bile duct; ERCP: Endoscopic retrograde cholangio pancreatography
regression. Statistical analyses of the data in this study were performed using SPSS software, version 17 (Chicago, IL).
RESULTS From August 2012 to September 2014, a total of 1296 patients underwent ERCP at Gastrointestinal Surgical Center, Mansoura University, Egypt. The study population consisted of 996 cases after exclusion of those who presented with obstructed stent (n = 66), active pan creatitis (n = 24), previous endoscopic sphinterotomy (n = 110), biliary complications after liver transplantation (n = 36), dye allergy (n = 10), pregnancy (n = 14), or mental disability (n = 10). Indications for ERCP were malignant obstructive
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El Nakeeb et al . Post-ERCP pancreatitis Table 2 Predictors of severity of pancreatitis after endoscopic retrograde cholangiopancrea tography n (%)
Patient related factors Median age (yr) Age < 35 > 35 Sex Male Female Median serum bilirubin (mg%) 2 Median CBD diameter (mm) < 10 > 10 Indication for ERCP Malignant Benign Type of papilla Normal Atrophic Pregnant Tumour Redundant Juxtadivericular Small Long Procedure related factors No. of cannulation attempts 3 times Method of cannulation Conventional Precut Biliary sphincter balloon dilatation No Yes
Mild to moderate pancreatitis (80)
Severe pancreatitis (22)
P -value
52
30
0.0001
26 (32.5) 54 (67.5)
14 (63.6) 8 (36.4)
0.0001
38 (47.5) 42 (52.5) 14.1 8 (50) 72 (85.7) 10 42 (52.5) 38 (47.5)
6 (27.3) 16 (72.7) 9.9 8 (50) 14 (14.3) 9 16 (72.7%) 6 (27.3%)
39 (97.5) 41 (66.1)
1 (2.5) 21 (33.9)
0.009
39 6 0 4 9 15 2 2
17 2 2 0 3 1 0 0
0.06
46 (57.5) 34 (27.5) 2 58 (72.5) 22 (52.4)
12 (54.5) 10 (45.5) 4 2 (9.1) 20 (90.9)
0.03
58 (72.5) 22 (52.4)
18 (81.8) 4 (18.2)
0.07
70 (87.5) 10 (12.5)
16 (72.7) 6 (27.3)
0.1
0.08 0.3 0.07 0.0001 0.0001
0.0001 0.0001
CBD: Common bile duct; ERCP: Endoscopic retrograde cholangiopancreatography.
Table 3 Multivariate logistic regression for analysis of pancreatitis after endoscopic retrograde cholangiopancreatography Variable Age group Age Sex CBD diameter below 10 mm CBD diameter Difficult cannulation No. of pancreatic cannulations below 3 No. of pancreatic cannulations Papilla
P -value
Odds ratio
0.001 0.519 0.362 0.609 0.000 0.207 0.117 0.000 0.964
0.035 1.012 0.143 0.726 0.612 0.476 0.219 5.258
95%CI for EXP(B) Lower
Upper
0.005 0.976 0.075 0.212 0.495 0.150 0.033 2.665
0.259 1.050 0.270 2.481 0.757 1.506 1.460 10.370
CBD: Common bile duct.
(8%) patients, while severe PEP occurred in 22 (2.2%) patients. These ratios are concordant with data reported [14-16] by previous studies .
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Among different patient related risk factors, younger age and non-dilated extrahepatic biliary radicals were independent risk factors for PEP on multivariate analysis
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El Nakeeb et al . Post-ERCP pancreatitis in this study. Also, using a cutoff value of 35 years to divide patients into two groups, the rate of PEP was significantly higher in the younger group by univariate analysis. Younger age has been a subject of controversy [8] regarding its association with PEP . Many studies reported an insignificant relation between patient age [2,17] [18] and likelihood of PEP . However, Freeman et al first reported relatively younger age as a predictor of PEP on multivariate analysis. This finding was confirmed [5,16,19] by later studies . Higher incidence of PEP in youn ger age was explained by the aging effect on pan creatic exocrine function, smaller common bile duct diameter and the higher incidence of sphincter of Oddi [13,16,18] dysfunction in younger age . Management of CBD stones in case of non-dilated extrahepatic biliary system represents a surgical cha [20] llenge . Laparoscopic transcholedochal CBD exploration [21-23] . mandates a CBD diameter of at least 6-8 mm According to many studies including this one, normal caliber CBD is associated with increased difficulty of the [24-26] ERCP procedure . However, most of recent studies reported absence of association between narrower [13] CBD diameter and PEP . Laparoscopic management for surgically fit patients with concomitant gall bladder and CBD stones in case of non-dilated CBD through transcystic CBD exploration or laparoendoscopic Rendez[21] vous is better to avoid or minimize the risk of PEP . In case of isolated choledocholithiasis or in patients who are unfit for surgery, prophylactic measures against PEP should be adopted. In this cohort, difficult cannulation, denoted by fre quent cannulation attempts and pancreatic cannulation more than three times, was associated with a higher risk of PEP. The effect of pancreatic duct injection with contrast dye on PEP could not be evaluated because we did not use the conventional contrast cannulation method. The effect of precut sphincterotomy on PEP [11] is controversial . Some authors advocate that precut sphincterotomy causes papillary oedema which retains [8,24] pancreatic secretion resulting in PEP . On the other hand, some authors indicate that precut sphincterotomy is usually preceded by difficult cannulation through the conventional approach and that the later, not the precut sphincterotomy itself, is responsible for the development [26] of PEP . This is supported by the finding that precut sphinctertomy was not reported as a risk factor for PEP from endoscopists who adopted precut sphincterotomy as a preferred technique from the start not just a salvage procedure after difficult cannulation through conven [27] tional cannulation methods . Early precut leads to more successful cannulation rate without more hazard of [28-33] morbidity after ERCP . [8] Risk factors for PEP have a synergetic effect . [1] Jeurnink et al suggested that development of pro gnostic models and scoring systems based on various patient and procedure related risk factors will help in defining patients at the highest risk for PEP. According to this cohort, young patients (< 35 years) with narrow CBD (< 10 mm) who had shown evidence of difficult
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cannulation (high number of cannulation attempts or pancreatic cannulation more than three times) are can didates for prophylactic and preventive measures against [28] PEP . Despite the improvement of techniques of ERCP in recent years and increased experiences, the incidence of PEP has not decreased. Therefore, studies to determine risky patients and predict severity of PEP are very important to give the risk factors prophylactic agents for [34-37] prevention of PEP . Pre-ERCP administration of rectal indometacin reduced the overall occurrence of PEP without [34] increasing risk of bleeding . Some studies reported that the combination of a temporary prophylactic pancreatic plastic stent placement and rectal non-steroidal antiinflammatory drugs is recommended for preventing PEP [34-36] in high-risk cases . Somatostatin can reduce the incidence of PEP but has not been routinely administrated in most of centers nor recommended by guidelines as a [36,37] prophylactic measure for PEP . Patients at high risk of PEP should be also monitored for at least 24 h to avoid [1,7] occurrence of PEP after early discharge . In conclusion, PEP is the most frequent and devastating complication after ERCP. PEP is associated with higher morbidity and mortality beside its effect in increasing the consumption of hospital resources. Age less than 35 years, narrower median CBD diameter and increased number of pancreatic cannulations are independent risk factors for the occurrence of PEP. Patients with these risk factors are candidates for prophylactic and preventive measures against PEP.
COMMENTS COMMENTS Background
Endoscopic retrograde cholangiopancreatography (ERCP) is increasingly used for therapeutic management of various biliary and pancreatic diseases. However, ERCP is not a procedure without morbidities. Post-ERCP pancreatitis (PEP) remains the most common and serious complication after ERCP. The reported incidence of PEP is around 5%. This rate may increase up to 20%-40% in high risk patients. Identification of risk factors for PEP helps adopt prophylactic measures in high risk patients and early discharge in low risk patients.
Research frontiers
Many studies have tried to identify the risk factors for pancreatitis after ERCP. Many patient and procedure related factors are suggested to be associated with increased likelihood of PEP. The trigger mechanism and pathogenesis for PEP remain unclear.
Innovations and breakthroughs
ERCP is not a procedure without morbidities. Identification of risk factors for PEP helps adopt prophylactic measures in high risk patients and early discharge in low risk patients.
Applications
The data in this study suggested risk factors for PEP and investigated the predictors of its severity in a tertiary high volume. Furthermore, this study also provided readers with important information regarding the risk factors for PEP.
Terminology
PEP remains the most devastating and frequent complication after ERCP. The reported incidence of PEP is around 5%. This rate may increase up to
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Peer-review
This is an interesting manuscript with a significant number of patients treating an important topic, and the aim of this study was to detect risk factors for PEP and investigate the predictors of its severity in a tertiary high volume referral surgical center in Egypt.
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papillotomy and fistulotomy improved the treatment outcome of patients with difficult biliary cannulation. Surg Endosc 2016; Epub ahead of print [PMID: 27129550 DOI: 10.1007/s00464-0164914-x] Ayoubi M, Sansoè G, Leone N, Castellino F. Comparison between needle-knife fistulotomy and standard cannulation in ERCP. World J Gastrointest Endosc 2012; 4: 398-404 [PMID: 23125897 DOI: 10.4253/wjge.v4.i9.398] Swan MP, Alexander S, Moss A, Williams SJ, Ruppin D, Hope R, Bourke MJ. Needle knife sphincterotomy does not increase the risk of pancreatitis in patients with difficult biliary cannulation. Clin Gastroenterol Hepatol 2013; 11: 430-436.e1 [PMID: 23313840 DOI: 10.1016/j.cgh.2012.12.017] Jin YJ, Jeong S, Lee DH. Utility of needle-knife fistulotomy as an initial method of biliary cannulation to prevent post-ERCP pancreatitis in a highly selected at-risk group: a single-arm prospective feasibility study. Gastrointest Endosc 2016; 84: 808-813 [PMID: 27102829 DOI: 10.1016/j.gie.2016.04.011] Mariani A, Di Leo M, Giardullo N, Giussani A, Marini M, Buffoli F, Cipolletta L, Radaelli F, Ravelli P, Lombardi G, D’Onofrio V, Macchiarelli R, Iiritano E, Le Grazie M, Pantaleo G, Testoni PA. Early precut sphincterotomy for difficult biliary access to reduce post-ERCP pancreatitis: a randomized trial. Endoscopy 2016; 48: 530-535 [PMID: 26990509 DOI: 10.1055/s-0042-102250] Kim SJ, Kang DH, Kim HW, Choi CW, Park SB, Song BJ, Hong YM. Needle-knife fistulotomy vs double-guidewire technique in patients with repetitive unintentional pancreatic cannulations.
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